Impaired body-centred sensorimotor transformations in congenitally deaf people

Abstract

Abstract Congenital deafness modifies an individual’s daily interaction with the environment and alters the fundamental perception of the external world. How congenital deafness shapes the interface between the internal and external worlds remains poorly understood. To interact efficiently with the external world, visuospatial representations of external target objects need to be effectively transformed into sensorimotor representations with reference to the body. Here, we tested the hypothesis that egocentric body-centred sensorimotor transformation is impaired in congenital deafness. Consistent with this hypothesis, we found that congenital deafness induced impairments in egocentric judgements, associating the external objects with the internal body. These impairments were due to deficient body-centred sensorimotor transformation per se, rather than the reduced fidelity of the visuospatial representations of the egocentric positions. At the neural level, we first replicated the previously well-documented critical involvement of the frontoparietal network in egocentric processing, in both congenitally deaf participants and hearing controls. However, both the strength of neural activity and the intra-network connectivity within the frontoparietal network alone could not account for egocentric performance variance. Instead, the inter-network connectivity between the task-positive frontoparietal network and the task-negative default-mode network was significantly correlated with egocentric performance: the more cross-talking between them, the worse the egocentric judgement. Accordingly, the impaired egocentric performance in the deaf group was related to increased inter-network connectivity between the frontoparietal network and the default-mode network and decreased intra-network connectivity within the default-mode network. The altered neural network dynamics in congenital deafness were observed for both evoked neural activity during egocentric processing and intrinsic neural activity during rest. Our findings thus not only demonstrate the optimal network configurations between the task-positive and -negative neural networks underlying coherent body-centred sensorimotor transformations but also unravel a critical cause (i.e. impaired body-centred sensorimotor transformation) of a variety of hitherto unexplained difficulties in sensory-guided movements the deaf population experiences in their daily life.